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Development of the foregut in Katharina tunicata (Mollusca; Polyplacophora)

Brandy S. Biggar

Posted on: 6 April 2021

Preprint posted on 28 February 2021

Say “Aaaah!”. Foregut development and toothed tongues in the black Katy chiton

Selected by Paul Gerald L. Sanchez and Stefano Vianello

Background

With the exception of bivalves (think mussels, scallops, and the sort) all 100000 species of molluscs that exist on our planet use the same structure for feeding: the radula (“little scraper”). This structure is a spikey, toothy, metal-studded “tongue”, through which snails, sea slugs, limpets and other molluscs graze their environment and sweep food into their digestive system.

The radula of the black Katy chiton (Katharina tunicata; Figure 1) is more of a mix between a drill, a chainsaw, and a conveyor belt, with up to 150 rows of mineral-hardened teeth excavating sediment and unearthing food. Developmentally, this structure is formed by outpocketing of the digestive tube of the larva, as the chiton settles to the seafloor to undergo metamorphosis and as its foregut transforms in the various components of the mouth cavity.  

Given the basal position of chitons within the mollusc evolutionary tree, studying the development of their feeding structures can hold important clues  about the life history of ancestral molluscs. Specifically, it is still unclear whether molluscan ancestors first lived their life floating and feeding in water (and then evolved to settle and live on the seabed), or whether they existed as seabed-dwellers that then evolved non-feeding larval forms, living in suspension. In this second scenario, the presence of feeding structures in the larvae would be a secondary evolutionary innovation and studies of basal species such as chitons can help resolve the directionality of such evolutionary changes.

 

Katharina tunicata post-metamorphic juveniles on encrusting coralline red algae

FIGURE 1:  Katharina tunicata post-metamorphic juveniles on encrusting coralline red algae A, B) 1 day post metamorphosis (dpm), C) 3 dpm, D) 14 dpm and E, F) 36 dpm. (from Figure 16 of the preprint, reproduced under CC-BY 4.0)

 

Key findings

This preprint combines external descriptions of Katharina tunicata development, and histology sectioning documenting important changes in internal anatomical features. Specific attention is given to foregut development, from larval stages to juvenile stages, through metamorphosis (Figure 2). Notably:

  • The author documents the presence of a differentiating buccal mass and radula already at 10 days post hatching. After one week, a radular rudiment and radular teeth can be observed in the larva.
  • As the larva settles on the seabed and undergoes metamorphosis into its armored juvenile form, the author describes the unique chiton process of biomineralisation of the radular teeth, which get capped with magnetite (!), and times this to occur at 14 days post-metamorphosis.

 

Katharina tunicata development and foregut ontogenesis through metamorphosis

FIGURE 2: Katharina tunicata development and foregut ontogenesis through metamorphosis. DPH: days post-hatching, DPM: days post-metamorphosis;  at: apical tuft; pr: prototroch, mt (or m): mouth; mg: midgut; bm: buccal mass; rr: radular rudiment; ne: neuropil; sv: shell valves; es: esophagus, mc: magnetite caps; rd: radula (adapted from preprint, reproduced under CC-BY 4.0)

 

Significance

This preprint provides detailed descriptions of internal anatomical changes in a Polyplacophoran species, going beyond simple external observation. Specifically, it provides a description of foregut development before, during, and after metamorphosis, leveraging the evolutionary position of this animal to provide insight on the possible features of ancestral molluscs.

Of note is the documentation of feeding structures (radula, buccal mass) already at the larval stage, even though Katharina tunicata larvae are non-feeding and rely on the yolk provided by the mother. If the black Katy chiton indeed preserves features of the common mollusc ancestor, the evidence gathered by this study supports a so-called “intercalation theory” of mollusc evolution whereas feeding larvae would be a secondary innovation and ancestral molluscs would have been seafloor dwellers. 

 

Questions to the author

  1. What does working with chitons look like in practice? Do you raise larvae in the lab?
  2. Why would a planktonic lifestyle favour evolvability of the foregut? Are there evolutionary pressures that would push a larva feeding on material yolk to develop structures to feed autonomously? 
  3. If a seafloor-dwelling lifestyle with non-feeding larvae was the ancestral condition, what would have pushed current planktonic mollusc species to abandon this lifestyle?
  4. Could you elaborate on the modularity of radulae in chitons and polyplacophorans? You mention that the chiton radula has a mix of features of other species.
  5. In e.g. mice and humans the foregut also originates the respiratory system. Is this the case also in molluscs?

 

Further reading

Page, L.R., and Hookham, B. 2017. The gastropod foregut- evolution viewed through a developmental lens. CJZ Virtual Spec. Issues 01:227–238.

Page, L.R. 2009. Molluscan Larvae: Pelagic juveniles or slowly metamorphosing larvae? Biol. Bull. 216:216–225.

iNaturalist entry of the Black Katy chiton: https://www.inaturalist.org/taxa/47632-Katharina-tunicata 

Tags: chiton, foregut, radula

doi: Pending

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